Behavioral Ecology doi:10.1093/beheco/ars021 Advance Access publication 13 March 2012

Original Article Male and female aggression: lessons from sex, rank, age, and injury in olive

a,b b,c d e b

Holly A. MacCormick, Daniel R. MacNulty, Anna L. Bosacker, Clarence Lehman, Andrea Bailey, Downloaded from D. Anthony Collins,f and Craig Packerb aDepartment of Ecology and Evolutionary Biology, Center for Ocean Health, University of California, 100 Shaffer Road, Santa Cruz, CA 95060, USA, bDepartment of Ecology, Evolution, and Behavior, University of Minnesota, 1987 Upper Buford Circle, St Paul, MN 55108, USA, cDepartment of Wildland Resources, d

Utah State University, 5230 Old Main Hill, Logan, UT 84322, USA, Department of Biology, Carleton http://beheco.oxfordjournals.org/ College, 1 North College Street, Northfield, MN 55057, USA, eCollege of Biological Sciences, 123 Snyder Hall, 1474 Gortner Avenue, Saint Paul, MN 55108, USA, and fGombe Stream Research Center, PO Box 185, Kigoma,

Aggression is ubiquitous, influencing reproduction through inter- and intraspecific effects in ways that reflect life-history strat- egies of species. In many social , females remain in their natal group for life, whereas males emigrate and compete for rank in other social groups. Competition for rank is inherently risky. Therefore, it has long been hypothesized that risks of injury depend on an individual’s sex, rank, and age in ways that maximize an individual’s reproductive output. However, studies quantifying such risks have been lacking. We analyzed 20 years of long-term data on wounds among olive baboons (Papio anubis) at Materials Acquisitions Dept., University Libraries on May 25, 2012 in Gombe National Park, Tanzania. Males received significantly more wounds than female baboons, and both sexes received the most wounds at ages when they competed most intensely for rank. Immature females received more wounds than immature males in their natal groups, and immature females were more likely to be wounded by females than were immature males. Males in their natal group were wounded less often than immigrant males of the same age. The risk of wounding did not depend on rank in females but rose with rank in immigrant males. Lastly, females received significantly more wounds when cycling (not pregnant or lactating). This study is among the first to quantify the risk of injury for competitors of different sexes, ages, and ranks in social groups. Our results support the prediction that individuals target aggression toward present and future compet- itors and suggest that sexual coercion increases the risk of wounding in cycling females. Key words: competition, injury, life history, olive , Papio anubis, rank. [Behav Ecol 23:684–691 (2012)]

INTRODUCTION for life (i.e., ‘‘female philopatry’’), whereas males immigrate into preexisting groups at puberty (i.e., ‘‘male-biased natal ompetition and sex are inextricably linked. This linkage dispersal’’) (Packer 1979a; Greenwood 1980; Dobson 1982; broadly spans taxa and affects the very structure and C Waser and Jones 1983). evolutionary dynamics of species. In social species, the relation- In many female-philopatric species, female rank is largely de- ship between competition and sex depends on such factors as termined by birth order and maternal rank (Kawamura 1958; reproductive strategies of the sexes, age and social rank of indi- Koford 1963; Koyama 1967; Cheney 1977; Holekamp and Smale viduals, and the life history of the species. Studies of related 1991). In contrast, male rank rises or falls according to the phenomena include (Clutton-Brock and Harvey outcome of pairwise interactions between males that reflect 1977; Muller and Wrangham 2009), birds (Wiley 1974; Arcese the competitor’s body size and physical condition (Hausfater 1989), rodents (Dobson 1982; Edelman 2011), carnivores 1975; Packer 1979b; van Noordwijk and van Schaik 1988; Haley (Bekoff et al. 1984), ungulates (Andersen et al. 2000), insects et al. 1994; Pelletier and Festa-Bianchet 2006). High-ranking (Kemp and Alcock 2003), and arachnids (Ulbrich and Henschel males have preferential access to females in many social mam- 1999). However, comparatively few studies have directly quanti- malian species with dominance hierarchies (e.g., LeBoeuf 1974; fied the risks of competition by linking competition with the Clutton-Brock et al. 1982; Moore et al. 1995; Constable et al. incidence of physical wounding. Social mammals, specifically 2001; Alberts et al. 2003; Natoli et al. 2007; Altmann et al. 2010). primates, provide an excellent system to explore this question However, individuals in their natal group often show reduced because of differences between the sexes that apply to many sexual attraction toward close kin (Packer 1979a; Pusey 1980; social mammalian species; females remain in their natal group Bolhuis et al. 1988; Simmons 1991; Manson and Perry 1993; Sterck et al. 2005). Thus, males typically do not engage in intra- Address correspondence to H.A. MacCormick. E-mail: maccormick@ sexual competition for females until dispersing to new groups biology.ucsc.edu. (Packer 1979a; Pusey and Packer 1987). As physical condition Received 9 February 2011; revised 25 August 2011; accepted 26 declines with age, older male baboons rely less on direct con- November 2011. frontation with high-ranking peers to obtain mating opportuni- ties and instead adopt alternative strategies such as forming The Author 2012. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: [email protected] MacCormick et al. • The effect of age, sex, and rank on the risk of injury in olive baboons 685 coalitions with other subordinate males and cultivating relation- METHODS ships with individual females (DeVore 1965; Packer 1977; Smuts Study area and population 1985; Bercovitch 1986, 1988; Noe¨ and Sluijter 1990; Alberts et al. 2003). Thus, direct aggressive competition is often most Gombe National Park, Tanzania, is comprised of a chain of intense between young, high-ranking immigrant males (Packer steep valleys flanked by Lake Tanganyika to the west and a rift 1979b; Yoccoz et al. 2002; Mainguy and Coˆte 2008). escarpment to the east (van Lawick-Goodall 1968; Packer Competition among females generally involves access to 1979a). A total of 671 male and 471 female baboons from resources rather than mates (Trivers 1972). Female per capita 12 different groups (hereafter ‘‘troops’’) have been studied reproductive success often declines with increasing group size since 1967; demographic data have been recorded daily since (van Noordwijk and van Schaik 1999 []; Packer et al. 1972 (Packer et al. 1998). 2000 [olive baboons]; Altmann and Alberts 2003 [Papio spp.]). Thus, infant females often represent future competi-

Wounding and dominance data Downloaded from tion for adult females, whereas infant males will eventually disperse to compete elsewhere. Therefore, adult females are Data on wounding and dominance rank are available from expected to employ behaviors that limit the survival of unre- January 1983 to November 2001. Tanzanian field assistants col- lated juvenile females, though documented examples of adult lected all data under the supervision of D.A.C. with assistance females selectively harassing immature females remain rare from A.B. ‘‘Wounds’’are defined as gashes, cuts, or punctures of (for toque [Macaca s. sinica] and bonnet [Macaca radiata] the skin. Monthly reports provide details on the date and num- macaques, e.g., Dittus 1979; Silk et al. 1981). ber of wounds for each baboon and indicate the cause of http://beheco.oxfordjournals.org/ Studies of intersexual aggression suggest that males are the wounding when witnessed (93 of 2078 cases of wounding). predominant aggressor and disproportionately wound females In addition to monthly reports, daily demographic records also (Muller and Wrangham 2009). Smuts (1985) found that female note the number of fresh wounds. Analyses where the sex of the olive baboons were the targets of male aggression approxi- attacker is known, and those assessing sexual coercion, are done mately once every 17 h. Adult male olive baboons are formida- separately for the number of wounding events and the number ble opponents, and males are approximately twice as large as of wounds received in a year. ‘‘Wounding events’’ are defined as females and have canines about a third longer and wider than the occurrence of one or more wounds on a single day. A dis- females (Virgadamo et al. 1972). Male olive baboons are also tinction is drawn between annual wounding events and the an- formidable relative to other . Male baboons have canine nual number of wounds because the likelihood of receiving teeth whose relative size can exceed those of felids, and pri- a wounding event versus several wounds at once may vary for mates in general can have canine teeth that are as long as individuals of different sexes, ages, and ranks. An individual at Materials Acquisitions Dept., University Libraries on May 25, 2012 carnivores, relative to their body size (Lucas 1982; Plavcan may receive many wounds in a single aggressive encounter or and Ruff 2008). Females may be at greater risk of wounding may receive few wounds in multiple aggressive encounters over during particular times if their reproductive state (e.g., cycling, the course of several different days. In all other analyses, wound- consorting with males, etc.) alters their frequency and/or type ing was scored as a binary outcome (yes/no) for every individ- of interactions with males. Olive baboons are one of many ual, for each year of the study. species that exhibit sexual dimorphism; therefore, the poten- Injuries typically persisted for weeks or months, although the tial costs of mating are of particular interest given the dispar- act of wounding was rarely observed. Contact with humans is ities between male and female body size and weaponry and the minimal at Gombe: all study troops have restricted home potential for males to monopolize and sexually coerce females ranges in the center of the national park and are completely (Clutton-Brock and Parker 1995; Muller and Wrangham 2009). isolated from local villagers. Human contact was limited to the Agonistic interactions between individuals inevitably involve Jane Goodall Institute research staff, Tanzania National Park risks of physical injury (Clutton-Brock et al. 1979; Blanchard staff, tourists, and itinerant local fisherman. All staff were et al. 1988; Drews 1996). Aggressive encounters are potentially strictly prohibited from harassing the baboons, and tourists the most costly between young adult males that are fully must maintain a distance of at least 10 m from wildlife. Al- grown and have not yet worn down their weapons (Packer though human-caused injuries were recorded, they were easily 1979b). Yet, measuring the costs of agonistic interactions in identifiable (e.g., by gunshot, snare) and extremely rare: only natural populations is difficult (Smuts BB and Smuts RW 10 cases out of 2078 wounding events. Of these 10 wounds, 3 1993; Mitani et al. 1996). In this paper, we analyze the age-, baboons were killed after humans had been attacked, 2 were sex-, and rank-specific risks of wounding in a long-term field injured after stealing food and destroying property, 2 were in- study of olive baboons (Papio anubis) in Gombe National Park, jured after stealing fish from fisherman, 1 was shot by park Tanzania, to test the following hypotheses: 1) If wounding rangers, and the remaining 2 were injured for unknown rea- differs between sexes, males should receive more wounds than sons. Although, chimpanzee-inflicted wounds can be similar females. 2) If wounding differs among individuals of different to baboon-inflicted wounds, the Gombe chimpanzees are sub- ages, males should receive most wounds during ages that ject to such intensive observation that chimpanzee attacks on correspond to times when males compete most intensely for baboons are well documented and could be excluded from the dominance rank and receptive females; females should re- analysis. Although present in Gombe, are rare: In ceive most wounds when their rank is first determined as more than 20 years of daily field observations, there is no de- juveniles. 3) If competition, dominance rank, and wounding finitive evidence of a attack on either olive baboons or are linked, rank should predict wounding for males because chimpanzees (Wilson et al. 2004; Gombe Stream Research male dominance rank is determined by direct competition. Center, unpublished data). Wounds caused by accidents Note, we do not expect to see a clear relationship between (e.g., falling from a tree) were typically described as scrapes, wounding and rank in females because once a female’s rank swelling of limbs, and limping. To minimize the inclusion of is established, it remains relatively stable for life, reducing such injuries, we only included wounds that involve a break in female–female competition, and because injuries from males the skin, cut, or puncture in the total data set of 2047 wound could potentially obscure any possible effect of rank on risk of events. Thus, the vast majority of injuries in our analysis could wounding. 4) If female injuries are inflicted by sexual coer- be inferred to have resulted from bites by conspecifics. cion, adult females should receive most wounds when they Annual dominance ranks were determined by the outcomes are cycling. of pairwise interactions involving displacements from food 686 Behavioral Ecology

Table 1 approximately 6 months of cycling, 6 months of gestation, and The number of injured females and the total number of wounds 11 months of lactation. Female olive baboons reach menarche recorded for cycling (i.e., menstruating, with or without sexual around 4–5 years of age, and cycle until approximately 23 swellings, consorting), pregnant, or lactating females years of age, when their fertility declines and eventually ceases around 24 years of age (Smuts and Nicholson 1989; Packer Cycling Pregnant Lactating et al. 1998). Females included in the female reproductive state analysis were between 3 and 22 years of age. Analyses were Wound events . Adolescent females 35 2 1 conducted separately for adult ( 7 years of age) and adoles- Adult females 252 38 105 cent females (females that had reached menarche but were Total 287 40 108 6 years of age) because females typically reach menarche Expected wound events and then cycle for about 1–2 years before their first pregnancy Adolescent females 9.9 9.9 18.2 (i.e., ‘‘adolescent sterility’’) (Smuts and Nicholson 1989).

Adult females 103.0 103.0 188.9 Downloaded from Total 113.0 113.0 207.1 Wound counts Statistical Analysis Adolescent females 64 2 2 Annual wounding rates were scored repeatedly (up to 21 con- Adult females 432 72 170 Total 546 74 174 secutive years for some animals) for 887 individuals and ana- Expected wound counts lyzed using generalized linear mixed models (GLMMs) with Adolescent females 17.7 17.7 32.5 a binomial error distribution and with individual identity fitted http://beheco.oxfordjournals.org/ Adult females 175.8 175.8 322.3 as a random effect. All models included a compound symmetric Total 193.6 193.6 354.9 correlation structure, which assumed that all observations within individuals were equally correlated on average. Models were es- Analyses were conducted separately for adult (.7 years of age) and timated with adaptive Gaussian quadrature with parameters es- adolescent (females that had reached menarche but were 6 years of timated from maximum likelihood, and significance of effects age) females. Expected ratios for each of the categories were wasdeterminedbyanapproximatez-test. calculated according to average duration of time females spend in We used piecewise linear splines to test for nonlinear effects each reproductive state: 6 months of cycling, 6 months of gestation, of age (as measured in discrete 1-year increments) on the prob- and 11 months of lactation. Please note that the 35 of adolescent ability that an individual was wounded in a given year. Piecewise female cycling wound events are the sum of the following categories: splines consist of a covariate (e.g., age) defined over specified

flat (N = 10), (N = 21), consort (N = 1), and menses at Materials Acquisitions Dept., University Libraries on May 25, 2012 (N = 3). The 252 adult female cycling wound events are the sum of the segments (e.g., . and ,4 years old) and a response variable following categories: flat (N = 116), sexual swelling (N = 108), consort (wounding) that is a continuous function of the covariate over (N = 20), and menses (N = 16). The 64 adolescent female cycling all segments, but with different slopes in each segment (Marsh wound counts are the sum of the following categories: flat (N = 13), and Cormier 2002). Each line segment does not have its own sexual swelling (N = 45), consort (N = 2), and menses (N = 4). The 432 intercept; rather, a spline regression model includes only a sin- adult female cycling wound counts are the sum of the following gle intercept that is adjusted by the spline variable to accom- categories: flat (N = 217), sexual swelling (N = 159), consort (N = 35), modate a change in slope. This keeps the regression line and menses (N = 22). continuous (i.e., no breaks) even as the regression line pivots to change direction at the points (knots) where the segments join. We used splines to identify the threshold age beyond sources or overt aggression. Summaries of these interactions which the probability of wounding abruptly changes, similar consistently revealed linear rankings where the top-ranking to the way knot location is used in epidemiology to identify male/female dominated all other like-sexed individuals in ‘‘the threshold value of a risk factor for which the probability his/her troop, the second ranking male/female dominated of disease occurring suddenly changes’’ (Bessaoud et al. 2005, the remainder, and so on. Each individual’s annual numerical p. 2). rank was converted to a ‘‘relative rank’’ by finding D/(N 2 1), To determine the presence and position of age-specific where D = the number of like-sexed animals dominated by thresholds in wounding, we evaluated a set of competing that individual and N = number of like-sexed individuals in GLMMs for each of 3 demographic classes: female, natal male, that troop that year. Thus, top-ranked individuals would have and immigrant male. Each set included models with a single relative ranks of 1.0, whereas bottom-ranking individuals knot placed at 6–10 different ages (females 3–12 years; natal would have 0.0. These scores were sorted into 5 categories: males 2–7 years; immigrant males 6–15 years) and a model with 0.0–0.199, 0.2–0.399, 0.4–0.599, 0.6–0.799, and 0.8–1.0. no knot, representing the hypothesis of no threshold in wounding. We selected knots a priori according to the age dis- Female reproductive state tribution of each demographic class, which was consistent with To address when females were at greatest risk of injury, we guidelines for the efficient use of knots (Wold 1974; Eubank noted both the number of injured females and number of 1984). By definition, knots selected a priori are fixed (i.e., not wounds to females that were cycling, pregnant, or lactating. random variables) and are therefore not estimated as param- Note that the visual assessment of the presence of a sexual eters in models. We created variables containing a linear swelling when females are sexually receptive could be imper- spline for age with the MKSPLINE command in STATA fect, especially during times of transition between reproductive 10.1. The variables were constructed so that the estimated stages. Therefore, the ‘‘cycling’’ category consisted of females coefficients measure the slopes for each segment before and that 1) had sexual swellings, 2) were consorting with males after a given knot. (this occurred when females also had sexual swellings), 3) We conducted all analyses in STATA 10.1 and compared did not have obvious sexual swellings but were neither lactating GLMMs using information-theoretic statistics (Burnham and nor pregnant, and 4) were menstruating (there were compar- Anderson 2002). Our scope of inference concerned the pop- atively few females in this category, see Table 1). We then ulation, so we performed model selection using marginal calculated an expected ratio of injured females and wounds likelihoods. The most parsimonious model was the one with according to the typical time females spent in each reproduc- the lowest Akaike information criterion (adjusted for small tive state: the interbirth interval is about 23 months, including sample, AICc) and smallest DAICc. DAICc equals the AICc MacCormick et al. • The effect of age, sex, and rank on the risk of injury in olive baboons 687

for the model of interest minus the smallest AICc for the set of models being considered. The best model has a DAICc of zero, and models with DAICc ,2 are plausibly the best. We calculated population-averaged fitted values from best fit GLMMs by deriving marginal expectations of the responses averaged over the random effects but conditional on the ob- served covariates. We also used likelihood ratio statistics to test specific hypotheses among nested models, and results were considered significant at P , 0.05. To minimize effects of small sample size at advanced ages, we restricttheanalysistoageswherethesamplesizeexceeded20 individuals. Thus, the maximum age for females was 23 years, the maximum for natal males was 9 years, and the age of immi- Downloaded from grant males ranged from a minimum of 4 years to a maximum of 20 years.

RESULTS

Context of wounding http://beheco.oxfordjournals.org/ Wounding was observed at the time it occurred in 93 of 2078 wound events. Of the wounds of known cause, 66% were due to bites from other baboons (N = 62), 14% to attacks by chim- panzees (N = 13), 11% to attacks by humans (N = 10), and 9% to accidents (e.g., falling from a tree, N = 8). Wounding was not observed in the remaining 1985 wound events; however, human-caused injuries were both easily identifiable (i.e., a gunshot or snare) and, moreover, were likely to be rare due to very limited contact between humans and baboons.

The Gombe chimpanzees were subject to far more intensive at Materials Acquisitions Dept., University Libraries on May 25, 2012 observation than the baboons; thus, the percentage of chim- panzee-inflicted wounds was likely an overestimate (see Figure 1 METHODS). All baboon wounds known to be caused by Age-specific risk of wounding for (A) female, (B) natal male, and chimpanzees, humans, or accidents were excluded from sub- (C) immigrant male baboons. The number of individuals in each sequent analyses leaving a total of 2047 wound events in the analysis is (A) 327, (B) 300, and (C) 260. Solid lines are population- data set. Male baboons were wounded more often (wound averaged fitted values from best fit GLMM models, with dotted lines events where an ‘‘event’’ is a 24-h day: males N = 1197, females indicating pointwise 95% confidence intervals. The estimated N = 850) and received more wounds overall than females coefficients before and after each spline knot are (A) 0.29 6 0.04 (wounds: males N = 1440, females N = 1063). (P , 0.001) and 20.01 6 0.02 (P = 0.63); (B) 0.07 6 0.07 (P = 0.31) Wounding for all analyses was scored as a binary outcome. and 0.29 6 0.09 (P = 0.001); and (C) 0.77 6 0.13 (P , 0.001) and 6 This is a conservative measure as approximately 65% of all 0.04 0.03 (P = 0.13). Circles are observed frequencies across individuals within each age class and are provided merely as a visual wounded baboons suffered exactly 1 wound event per year. aid; analyses were performed on the raw binary data. Of ranked individuals that received 2 or more wound events per year, females received similar proportions of wounding Supplementary Material). None of the spline models fit the events for all rank classes, whereas the highest quintile of males female data well (DAICc  3.00). By contrast, spline models suffered the most wounding events per year (39%). with knots at age 9 and 10 provided the best and second The sex of the attacking baboon was known for 44 of the 62 best (DAICc = 1.11) fit, respectively, to the immigrant male data observed baboon-inflicted wounding events; the identity was (N = 192 ranked immigrant males), indicating that immigrant known for 42 of 62 events, where 21 injured baboons were male male rank peaks at age 9–10. Models with knots at ages ,9and and 23 were female. With the exception of one case where .10 performed poorly (DAICc . 14.00, Supplementary a mother wounded her son, these 21 males were wounded only Material). Before 9 years of age, the rank of immigrant males by other males. On the other hand, the 23 females were increased with age (slope = 0.75 6 0.09, P , 0.001); after wounded by both males (N = 16) and females (N = 7). For 9 years, immigrant male rank declined with age (slope = individuals ,6 years of age, females were more likely to be 20.18 6 0.02, P , 0.001). wounded by females (4 of 8 cases) than were males (1 of 9 cases) (P = 0.02, binomial test with p = q = 4/8). The relatively Wounding versus age small number of total female injuries in the ,6 years of age class may be attributed to stochasticity in a small sample size. The annual risk of wounding changed with age for all 3 age–sex classes. For females, the best model is given by a change in slope at 6 years of age: before the age of 6, risk of injury increased by Age versus rank 34% per year; thereafter, risk does not significantly change with The sex-specific relationship between dominance rank and age age (Figure 1A, Supplementary Material). Models of female confirmed prior studies of this same population (Packer et al. wounding with knots before or after age 6 did not perform 1995). Specifically, an intercept-only model provided the best well (DAICc . 3.50). For males in their natal troop, the best fit (DAICc = 0.00) to the female data (N = 155 ranked females), model is given by a change in slope at 4 years of age: risk of indicating that rank was constant across all ages in females. The injury is constant before the age of 4 and risks increased by next best model (DAICc = 1.71), which included a linear term 34% per year thereafter (Figure 1B, Supplementary Material). for age, was not significantly different from the intercept-only However, models of natal male wounding with either no model (v2 = 0.33, degrees of freedom [df] = 1, P =0.57, knot or knots at 3, 5, and 6 years of age also performed well 688 Behavioral Ecology

DISCUSSION Life-history theory posits that individuals will employ reproduc- tive strategies to maximize the number of offspring. Classical examples of extremes in life-history strategies are semelparous species that reproduce once and then die versus iteroparous spe- cies that reproduce periodically throughout a longer lifetime (Stearns 1976). This is not restricted to animals. For example, perennial species can develop long-lived roots and stems as investments for repeated seed crops, each crop of moderate size, whereas annuals spend all the year’s accrued energy in a single large seed crop. The extremes can be thought of as

long-term versus short-term reproductive strategies. Between Downloaded from Figure 2 the extremes, life histories can be categorized by means and Relationship between relative rank and the risk of wounding for males variances of parameters such as ages of first and last reproduc- (squares) and females (circles). Open symbols are observed frequencies tion, juvenile and adult survival, and fertility (Oli and Dobson across individuals with each rank and are provided as a visual aid; 2003). They are also conveniently summarized as varying de- analyses were performed on the raw binary data. Solid symbols are fitted grees of ‘‘capital’’ versus ‘‘income’’ strategies (Stephens et al. values with 95% confidence intervals from a GLMM model. 2009), where they often apply to stores of nutrients and body http://beheco.oxfordjournals.org/ tissues but can also apply to behaviors.

(DAICc , 2.00), indicating substantial uncertainty about the Life-history strategies are evolutionary responses to the presence and location of any age-specific change in the risk pervasive problem of maximizing reproductive success. They of injury for natal males. For immigrant males, the best model become particularly complex in social animals such as pri- is given by a change in slope at 8 years of age: risk of injury mates, where they can manifest as dominance hierarchies more than doubles each year from 4 to 8 years and is constant and persistent agonistic behaviors. Agonistic behaviors may thereafter (Figure 1C, Supplementary Material). The next best seem maladaptive because injuries can reduce reproductive model of immigrant male wounding included a knot at age success. Yet, aggressive behavior can be evolutionary adaptive 9years(DAICc = 2.56), whereas models with knots at ages if the risk of injury is countered by benefits such as preferential ,8or.9 years did not score well (DAICc . 6.00). access to resources and/or mates, immediately or in the future.

Despite recognition that life-history theory and its evolutionary at Materials Acquisitions Dept., University Libraries on May 25, 2012 origins can influence agonistic behaviors, empirical studies are Immature individuals: males and females few, and studies quantifying the risks of aggressive behavior are For all injuries in animals less than 6 years of age, females (N = largely theoretical (Smuts BB and Smuts RW 1993; Clutton- 291 individuals) were nearly twice as likely to be wounded Brock and Parker 1995). each year as same-aged natal males (N = 300 individuals) In olive baboons, 2 life-history strategies are female philopa- (odds ratio = 1.91 6 0.33, P , 0.001). try and male dispersal. Females remain in their natal group for life, whereas males immigrate into preexisting groups at pu- berty. Juvenile females largely inherit their place in the dom- Males: immigrants versus natal males inance hierarchy by acquiring a rank similar to that of their mother. Once established, a female’s rank remains relatively For all injuries in males between 4 and 9 years of age, immi- stable for life. In contrast, male olive baboons disperse to grants (N = 177 individuals) were 70% more likely to be new troops as juveniles and obtain and maintain their wounded each year than same-aged natal males (N = 148 in- position in the via direct competition be- dividuals) (odds ratio = 1.70 6 0.42, P = 0.03). Note that this tween males. The ability of rank to predict reproductive success analysis is based on a total of 264 individuals. Of these, 61 varies among different species of social animals (Pusey et al. males were measured both as natal and immigrant males, 1997). Smuts (1987) noted a positive relationship between having transferred from one study troop to another. high rank and reproductive success in many cercopithecine primates, and a study by Pusey et al. (1997) found that high- Wounding versus rank ranking female chimpanzees have ‘‘higher infant survival, fast- er maturing daughters, and more rapid production of young.’’ The risk of wounding each year was constant across female rank However, both Smuts (1987) and Pusey et al. (1997) note that categories (odds ratio = 1.07 6 0.06, P = 0.26, N = 155 ranked this is not true of all social mammals, citing a possible trade- females 23 years old; Figure 2) but increased by 32% for off between the benefits and costs of high rank (Pusey et al. each rank quintile in immigrant males (odds ratio = 1.32 6 1997). 0.09, P , 0.001, N = 192 ranked immigrant males 4–20 years In olive baboons, high-ranking females have shorter inter- old) (Figure 2). birth intervals (Smuts and Nicholson 1989). However, no re- lationship was found between a female’s dominance rank and infant survival, adult female mortality, or sex ratio at birth Sexual coercion (Smuts and Nicholson 1989). In contrast, high-ranking male Adult and adolescent females were far more likely to be olive baboons father significantly more offspring, likely be- wounded and received the most wounds while cycling than cause they are better able to compete for and monopolize when they were pregnant or lactating (Table 1, N = 433 estrous females (Packer 1979b). These studies suggest that wounded females; N = 742 wounds, chi-square test, adult male reproductive success may be more tightly coupled to females’ wound events v2 = 294, df = 2, P  0.001; adult their position in the dominance hierarchy because higher females’ number of wounds v2 = 507, df = 2, P  0.001; rank affords greater access to mates in males. For these rea- adolescent females’ wound events v2 = 86, v2 = 64, df = 2, sons, males are hypothesized to compete intensely for rank P  0.001; adolescent females’ wound counts v2 = 163, and access to females, whereas females are hypothesized to df = 2, P  0.001). compete most aggressively when females first establish rank as MacCormick et al. • The effect of age, sex, and rank on the risk of injury in olive baboons 689 juveniles and are predicted to be the target of injury via sexual chies are relatively stable reduces the need for competition coercion from males. among females. This may be an evolutionary adaptation to The findings of our study have direct counterparts in life- enhance reproductive success in species where infant survival history theory and its evolutionary origins. Immigrant males depends heavily on the consistency of maternal care. suffered more wounds than same-aged natal males. A male Asymmetries in male–male versus female–female aggression baboon’s initial attempts to transfer into a new troop are often cross the boundaries of taxa, possibly reaching even to humans. met with intense aggression by the new troop’s resident males Studies of human females suggest that women tend to engage in (Packer 1979a; Packer and Pusey 1979; Henzi and Lucas 1980; aggressive behavior and competition less than men (Campbell Cheney and Seyfarth 1983; van Noordwijk and van Schaik 1999). A common theme among mammals is that females pro- 1985; Zhao 1994). These new immigrants not only represent vide the majority of parental care (Clutton-Brock 1991). Given increased competition for resources and mates they may also the benefits of a stable dominance hierarchy which reduces the be infanticidal (Palombit 1999), creating high fitness stakes need for competition, a greater investment in parental care, for residents. Once wounded, transferring males may briefly and a possible evolutionary adaption toward self-preservation Downloaded from return to their natal troop before attempting to immigrate for the sake of higher infant survival, it is somewhat unsurpris- again (Packer 1979a). This period of dispersal corresponds ing that female olive baboons are wounded less frequently and to an increased risk of wounding for natal males above 4–5 with less severity than males and have a life-history strategy that years of age. Immigrant males that have already dispersed are helps ensure that. Moreover, in more than 20 years of field wounded most often. Among immigrant males, the highest observations, competition among females was a low-level, more ranking males suffer approximately twice as many wounds as chronic occurrence than that of male–male agonistic interac- http://beheco.oxfordjournals.org/ the lowest ranking males. Interestingly, the highest risk of tions (Gombe Stream Research Center, unpublished data). wounding was at 8 years of age, although males typically attain These observations are consistent with the patterns of wound- the highest rank of their life at 9 years of age. That suggests ing observed in this study. Wounds are fairly evenly distributed that young males are at the greatest risk of injury when they across all female rank classes. From an evolutionary adaptive first begin competing for top rank, not when they actually standpoint, the smaller female body size and unexaggerated attain the highest rank of their life. weaponry further suggest that competition and the ability to The subset of our data where the sex of the attacker was fight are not of paramount importance for females. Indeed, known is relatively small (21 injured males and 23 injured the opposite is important, the ability to avoid fighting and females), and we would like to have more data for the light maintain continuous intervals of parental care. it would shed on differences in aggression by sex. Nonetheless, In contrast, male dominance hierarchies are more dynamic 70% of observed injured females were wounded by males. Sex- than that of females, owing to the influx of immigrant males at Materials Acquisitions Dept., University Libraries on May 25, 2012 ually cycling females suffered by far the most wound events and and the movement of adult males between troops. The lack of the most wounds of any reproductive stage, suggesting that in- stability in dominance hierarchy perpetuates the need to fre- creased interactions with males during periods of sexual recep- quent competition to establish and reestablish the order of tivity account for the disproportionate risks of wounding. male rank. A less stable dominance hierarchy; the continual Dominance rank does not appear to influence the risk of influx of new males; females as a limiting resource; more for- wounding for females, a result that is somewhat surprising midable weaponry; a greater link between male reproductive given that prior studies of primates and other social mammals success, rank, and access to females; and perhaps a greater abil- indicate subordinate females often receive more aggression ity to adopt a more cavalier attitude toward survival beyond (Seyfarth 1976; Silk et al. 1981; Clutton-Brock and Parker mating (as infant survival depends less on paternal care) all 1995; Perry 1996; Clutton-Brock et al. 2006) and are sup- promote male competition that is of greater frequency and in- ported less often in agonistic encounters (Prud’Homme and tensity than that of females. Chapais 1993; Silk et al. 2004) than high-ranking females. In some species, life-history strategies and reproductive strat- This result may be due to the fact that females establish rank egies are one and the same. In primates, life-history strategies prior to reaching adulthood (Cheney 1977), and female hier- (e.g., female philopatry and male dispersal) and reproductive archies often remain stable for prolonged periods decreasing strategies are intertwined. Baboons and other social mammals the need to maintain rank through intense aggression. do not employ a single such strategy. In olive baboons, compe- Males are wounded more often than females at most ages, and tition between males for increased rank represents a long-term immigrant males are wounded most often. For females, most capital breeding strategy—an immediate risk of injury in ex- wounds occur in juveniles prior to the onset of menarche. Be- change for possibilities of future breeding. Concomitantly, co- yond adolescence (6 years of age and up), there is little relation- ercive attempts by males consorting with receptive females are ship between wounding and dominance in females. However, a short-term income breeding strategy, with immediate risks of data on wounds to females during different reproductive stages injury providing the possibility of immediate breeding success. did provide a way to quantify the potential costs of mating, and In contrast, the largely inherited dominance hierarchy of there is a strong relationship between cycling females and females is more representative of a different breeding strategy wounding, supporting the sexual coercion hypothesis. These entirely. Female reproductive success depends heavily on findings suggest that increased interactions with males when females surviving in good condition to give parental care females are sexually receptive account for the disproportionate and therefore aggression is less favored altogether. Thus, number and frequency of wounds to females. This result is par- the diametric breeding strategies of olive baboons both max- ticularly striking because the cycling stage is short, less than one- imize reproductive fitness but in different ways with respect to third of all reproductive stages combined. competition and wounding; the males’ strategies tolerate Our findings are consistent with the predictions based on wounds whereas the females’ strategy avoids them. olive baboon life-history patterns and social structure. Females This empirical study has provided some connections between invest more heavily in parental care; therefore, females are the the dual themes of behavior and life history in a species. limiting sex. As such, males are predicted to, and do, compete What may seem to be idiosyncratic primate behavior, studied for more intensely for access to females. This is evident by the its subtle intricacy and fascinating complexity, resides within greater frequency and severity of wounds received by males. a life-history perspective as a special case in the general theme The fact that female rank is largely inherited—something of organic reproduction and evolution, applying broadly across competition can do little to change—and dominance hierar- taxonomic groups from animals to . 690 Behavioral Ecology

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